Telomeres shorten and then lengthen before fledging in Magellanic penguins (Spheniscus magellanicus)

Cerchiara, Jack A.; Risques, Rosa Ana; Prunkard, Donna; Smith, Jeffrey R.; Kane, Olivia J.; Boersma, P. Dee

doi:10.18632/aging.101172

Cited by 12 publications

(14 citation statements)

References 61 publications

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“…Studies of terminal telomere restriction fragments (TRFs) have shown that telomere length can shorten with increasing age and that the rate of change corresponds to lifespan in several species (Bize, Criscuolo, Metcalfe, Nasir, & Monaghan, ; Juola, Haussmann, Dearborn, & Vleck, ; Tricola et al, ). However, this trend is not consistent amongst all birds, with some species showing increases in TRF with age, as in the Leach's storm‐petrel ( Oceanodroma leucorhoa ) (Haussmann et al, ), and no decline in length, or both as reported for the Magellanic penguin ( Spheniscus magellanicus ) (Cerchiara et al, ). For individuals in some avian species, change in telomere length can be tracked longitudinally and correlate with reproductive timing; however, the use of TRF for cross‐sectional analysis of age has yet to be demonstrated (Bauer et al, ).…”

Section: Discussionmentioning

confidence: 95%

Age estimation in a long‐lived seabird (Ardenna tenuirostris) using DNA methylation‐based biomarkers

Paoli-Iseppi

Deagle

Polanowski

et al. 2019

Molecular Ecology Resources

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Age structure is a fundamental aspect of animal population biology. Age is strongly related to individual physiological condition, reproductive potential and mortality rate. Currently, there are no robust molecular methods for age estimation in birds. Instead, individuals must be ringed as chicks to establish known‐age populations, which is a labour‐intensive and expensive process. The estimation of chronological age using DNA methylation (DNAm) is emerging as a robust approach in mammals including humans, mice and some non‐model species. Here, we quantified DNAm in whole blood samples from a total of 71 known‐age Short‐tailed shearwaters (Ardenna tenuirostris) using digital restriction enzyme analysis of methylation (DREAM). The DREAM method measures DNAm levels at thousands of CpG dinucleotides throughout the genome. We identified seven CpG sites with DNAm levels that correlated with age. A model based on these relationships estimated age with a mean difference of 2.8 years to known age, based on validation estimates from models created by repeated sampling of training and validation data subsets. Longitudinal observation of individuals re‐sampled over 1 or 2 years generally showed an increase in estimated age (6/7 cases). For the first time, we have shown that epigenetic changes with age can be detected in a wild bird. This approach should be of broad interest to researchers studying age biomarkers in non‐model species and will allow identification of markers that can be assessed using targeted techniques for accurate age estimation in large population studies.

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Section: Discussionmentioning

confidence: 95%

Age estimation in a long‐lived seabird (Ardenna tenuirostris) using DNA methylation‐based biomarkers

Paoli-Iseppi

Deagle

Polanowski

et al. 2019

Molecular Ecology Resources

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“…A meta‐analysis of 27 studies which measured TL at variable stages suggests that longer telomeres are associated with better survival (Wilbourn et al, ). Similarly, studies which investigate early‐life TL and survival have also demonstrated positive TL effects on short‐term survival (post growth period or fledging in birds (Geiger et al, ; Stier et al, ; Watson, Bolton, & Monaghan, )) or first year survival (Cram, Monaghan, Gillespie, & Clutton‐Brock, ; Salmón, Nilsson, Watson, Bensch, & Isaksson, ) but not always (Boonekamp, Mulder, Salomons, Dijkstra, & Verhulst, ; Cerchiara et al, ; McLennan et al, ; Stier et al, ; Ujvari & Madsen, ; Vedder et al, ). However, because extrinsic factors are always likely to be a major cause of mortality and TL‐associated mortality is likely to diminish with age (Boonekamp, Simons, Hemerik, & Verhulst, ), the predictive effect of early‐life TL on survival may be age‐dependent under natural conditions, a plausible yet untested hypothesis in the wild (Supporting Information Table ).…”

Section: Introductionmentioning

confidence: 97%

“…year survival (Cram, Monaghan, Gillespie, & Clutton-Brock, 2017;Salmón, Nilsson, Watson, Bensch, & Isaksson, 2017) but not always (Boonekamp, Mulder, Salomons, Dijkstra, & Verhulst, 2014;Cerchiara et al, 2017;McLennan et al, 2017;Stier et al, 2014;Ujvari & Madsen, 2009;Vedder et al, 2017). However, because extrinsic factors are always likely to be a major cause of mortality and TL-associated mortality is likely to diminish with age (Boonekamp, Simons, Hemerik, & Verhulst, 2013), the predictive effect of earlylife TL on survival may be age-dependent under natural conditions, a plausible yet untested hypothesis in the wild (Supporting Information Table S1).…”

mentioning

confidence: 99%

Early‐life telomere length predicts lifespan and lifetime reproductive success in a wild bird

et al. 2019

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Poor conditions during early development can initiate trade‐offs that favour current survival at the expense of somatic maintenance and subsequently, future reproduction. However, the mechanisms that link early and late life‐history are largely unknown. Recently it has been suggested that telomeres, the nucleoprotein structures at the terminal end of chromosomes, could link early‐life conditions to lifespan and fitness. In wild purple‐crowned fairy‐wrens, we combined measurements of nestling telomere length (TL) with detailed life‐history data to investigate whether early‐life TL predicts fitness prospects. Our study differs from previous studies in the completeness of our fitness estimates in a highly philopatric population. The association between TL and survival was age‐dependent with early‐life TL having a positive effect on lifespan only among individuals that survived their first year. Early‐life TL was not associated with the probability or age of gaining a breeding position. Interestingly, early‐life TL was positively related to breeding duration, contribution to population growth and lifetime reproductive success because of their association with lifespan. Thus, early‐life TL, which reflects growth, accumulated early‐life stress and inherited TL, predicted fitness in birds that reached adulthood but not noticeably among fledglings. These findings suggest that a lack of investment in somatic maintenance during development particularly affects late life performance. This study demonstrates that factors in early‐life are related to fitness prospects through lifespan, and suggests that the study of telomeres may provide insight into the underlying physiological mechanisms linking early‐ and late‐life performance and trade‐offs across a lifetime.

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“…We measured telomere length by quantitative polymerase chain reaction (qPCR), as in Cerchiara et al. (2017). …”

Section: Methodsmentioning

confidence: 99%

“…We extracted DNA from a lightly centrifuged cell pack, consisting primarily of erythrocytes (Qiagen DNeasy Mini-kit), and then quantified DNA via NanoDrop spectrophotometer (mean 260/280 ratio ± SE = 1.85 ± 0.02). We measured telomere length by quantitative polymerase chain reaction (qPCR), as in Cerchiara et al (2017).…”

Section: Sample Collection and Dna Extractionmentioning

confidence: 99%

Magellanic penguin telomeres do not shorten with age with increased reproductive effort, investment, and basal corticosterone

Cerchiara

Risques

Prunkard

et al. 2017

Ecology and Evolution

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All species should invest in systems that enhance longevity; however, a fundamental adult life‐history trade‐off exists between the metabolic resources allocated to maintenance and those allocated to reproduction. Long‐lived species will invest more in reproduction than in somatic maintenance as they age. We investigated this trade‐off by analyzing correlations among telomere length, reproductive effort and output, and basal corticosterone in Magellanic penguins (Spheniscus magellanicus). Telomeres shorten with age in most species studied to date, and may affect adult survival. High basal corticosterone is indicative of stressful conditions. Corticosterone, and stress, has been linked to telomere shortening in other species. Magellanic penguins are a particularly good model organism for this question as they are an unusually long‐lived species, exceeding their mass‐adjusted predicted lifespan by 26%. Contrary to our hypothesis, we found adults aged 5 years to over 24 years of age had similar telomere lengths. Telomeres of adults did not shorten over a 3‐year period, regardless of the age of the individual. Neither telomere length, nor the rate at which the telomeres changed over these 3 years, correlated with breeding frequency or investment. Older females also produced larger volume clutches until approximately 15 years old and larger eggs produced heavier fledglings. Furthermore, reproductive success (chicks fledged/eggs laid) is maintained as females aged. Basal corticosterone, however, was not correlated with telomere length in adults and suggests that low basal corticosterone may play a role in the telomere maintenance we observed. Basal corticosterone also declined during the breeding season and was positively correlated with the age of adult penguins. This higher basal corticosterone in older individuals, and consistent reproductive success, supports the prediction that Magellanic penguins invest more in reproduction as they age. Our results demonstrate that telomere maintenance may be a component of longevity even with increased reproductive effort, investment, and basal corticosterone.

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Telomeres shorten and then lengthen before fledging in Magellanic penguins (Spheniscus magellanicus)

Cited by 12 publications

References 61 publications

Age estimation in a long‐lived seabird (Ardenna tenuirostris) using DNA methylation‐based biomarkers

Age estimation in a long‐lived seabird (Ardenna tenuirostris) using DNA methylation‐based biomarkers

Early‐life telomere length predicts lifespan and lifetime reproductive success in a wild bird

Magellanic penguin telomeres do not shorten with age with increased reproductive effort, investment, and basal corticosterone

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